Cardiac and metabolic physiology of early larval zebrafish (Danio rerio) reflects parental swimming stamina

PHYSIOLOGY

ORIGINAL RESEARCH ARTICLE
published: 24 February 2012
doi: 10.3389/fphys.2012.00035

Cardiac and metabolic physiology of early larval zebrafish
(Danio rerio) reflects parental swimming stamina
Matthew Gore and Warren W. Burggren *
Developmental Integrative Biology Cluster, Department of Biological Sciences, University of North Texas, Denton, TX, USA

Edited by:
Richard Londraville, University of
Akron, USA
Reviewed by:
Brad Buckley, Portland State
University, USA
David Marcinek, University of
Washington, USA
Tim Moerland, Kent State University,
USA
*Correspondence:
Warren W Burggren, Department of
Biological Sciences, University of
North Texas, 1155 Union Circle
#305220, Denton, TX 76203, USA.
e-mail: burggren@unt.edu

Swimming stamina in adult fish is heritable, it is unknown if inherited traits that support
enhanced swimming stamina in offspring appear only in juveniles and/or adults, or if these
traits actually appear earlier in the morphologically quite different larvae. To answer this
question, mature adult zebrafish (Danio rerio) were subjected to a swimming performance
test that allowed separation into low swimming stamina or high swimming stamina groups.
Adults were then bred within their own performance groups. Larval offspring from each of
the two groups, designated high (LHSD) and low stamina-derived larvae (LLSD), were then
reared at 27C in aerated water (21% 02). Routine (fH,r) and active (fH,a) heart rate, and
routine (Mo2, r) and active (Mo2, a) mass-specific oxygen consumption were recorded
from 5 days post fertilization (dpf) through 21 dpf, and gross cost of transport and factor-
ial aerobic metabolic scope were derived from Mo2 measurements. Heart rate generally
ranged between 150 and 225 bpm in both LHSD and LLSD populations. However, significant
(P < 0.05) differences existed between the LLSD and LHSD populations at 5 and 14 dpf in fH,r
and at days 10 and 15 dpf in fH,a. /Mo2, r was 0.04-0.32 imol mg-1 h-1, while MO2, a was
0.2-1.2 imol mg-1 h-1. Significant (P < 0.05) differences between the LLSD and LHSD pop-
ulations in Mo2, r occurred at 7, 10, and 21 dpf and in Mo2, a at 7 dpf. Gross cost of transport
was ~6-10 imol 02.1g-1 m-1 at 5 dpf, peaking at 14-19 imol 02 g-1 m-1 at 7-10 dpf,
before falling again to 5-6 imol 02 g-1 m-1 at 21 dpf, with gross cost of transport signif-
icantly higher in the LLSD population at 7 dpf. Collectively, these data indicate that inherited
physiological differences known to contribute to enhanced stamina in adult parents also
appear in their larval offspring well before attainment of juvenile or adult features.
Keywords: zebrafish, cardio-respiratory physiology, inherited traits, swimming stamina

INTRODUCTION
Individual fishes capable of elevated swimming speeds and/or
showing enhanced stamina tend to exhibit longer lengths, have
a higher percentage of skeletal muscle as a proportion of total
body mass, and show higher metabolic scope for activity when
compared with other individuals from a general population (for
reviews, see Farrell, 2002; Claireaux et al., 2005; Claireaux and
Lefrangois, 2007; Farrell, 2007; Clark et al., 2011). While the mor-
phological and physiological underpinnings of enhanced loco-
motor performance in adult fish are well understood, relatively
few studies have considered these topics in larval fishes. How-
ever, the literature on the energetics and physiology of larval fish
locomotion has been expanding, driven by relevance to ecology,
environment, and aquaculture as well as fundamental physiologi-
cal questions (for an entry in to the literature, see Leis, 2006; Hurst
et al., 2007; Nilsson et al., 2007; MacPhail et al., 2009; Lindsey et al.,
2010; Colwill and Creton, 2011). Numerous studies, often on lar-
val zebrafish, have begun to reveal the interrelationships between
metabolic activity, swimming patterns during development, and
developmental changes in heart and axial muscle development
(see for example Mtiller et al., 2000; Bagatto et al., 2001; Pelster
et al., 2003; Muliiler and van Leeuwen, 2004; Thorsen et al., 2004;
van der Meulen et al., 2006; McLean and Fetcho, 2009).

Despite this expansion of studies on the locomotory energetics
and physiology of larval fish, most studies on the heritability of
fish locomotor energetics and mechanics have remained focused
on adult stages - either as adult parents or adult offspring. Elevated
swimming performance in fishes is certainly a heritable trait sub-
ject to natural selection (e.g., Evans et al., 2004; Langerhans et al.,
2004). For example, Langerhans et al. (2004) demonstrated that
populations of mosquito fish (Gambusia affinis) subjected to high
levels of predation had evolved a larger caudal fin, longer body, a
more ventral-posterior eye location, and faster burst speeds, when
compared to populations that experience lower predation levels.
These morphological differences persisted into subsequent gen-
erations, suggesting a heritable component to these modifications
for improved locomotor performance and prey avoidance. There is
some evidence that not just the trait of elevated swim performance,
but also degraded swim performance, can cross generations. For
example, the parr stage of sockeye salmon (Oncorhynchus nerka)
show degraded swimming performance when derived from adult
females that were moribund at the end of migration for spawn-
ing (Tierney et al., 2009). Offspring growth was not affected, but
physiological indicators such as plasma lactate concentration in
post-exercise state, typically used as an indicator of white mus-
cle use, was greater for parr derived from moribund adult females.

February 2012 I Volume 3 I Article 35 I 1

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Gore, Matthew & Burggren, Warren W. Cardiac and metabolic physiology of early larval zebrafish (Danio rerio) reflects parental swimming stamina. [Lausanne, Switzerland]. UNT Digital Library. http://digital.library.unt.edu/ark:/67531/metadc115198/. Accessed August 22, 2014.